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Biological effects of exposure to magnetic resonance imaging: anoverview

Domenico Formica and Sergio Silvestri* Address: School of Biomedical Engineering, "Campus Bio-Medico" Via Longoni 83 - 00155, Rome, Italy

Email: Domenico Formica - [email protected]; Sergio Silvestri* - [email protected]

* Corresponding author

Abstract

The literature on biological effects of magnetic and electromagnetic fields commonly utilized in

magnetic resonance imaging systems is surveyed here. After an introduction on the basic principles

of magnetic resonance imaging and the electric and magnetic properties of biological tissues, the

basic phenomena to understand the bio-effects are described in classical terms. Values of field

strengths and frequencies commonly utilized in these diagnostic systems are reported in order toallow the integration of the specific literature on the bio-effects produced by magnetic resonance

systems with the vast literature concerning the bio-effects produced by electromagnetic fields. This

work gives an overview of the findings about the safety concerns of exposure to static magnetic

fields, radio-frequency fields, and time varying magnetic field gradients, focusing primarily on thephysics of the interactions between these electromagnetic fields and biological matter. The

scientific literature is summarized, integrated, and critically analyzed with the help of authoritative

reviews by recognized experts, international safety guidelines are also cited.

IntroductionSafety issues and discussions about potential hazardsassociated with magnetic resonance imaging (MRI) sys-tems and procedures have been extremely controversialover the past decade: partly because of the disputed asser-tions about the role of electromagnetic fields in carcino-

genesis or the promotion of abnormalities in growth anddevelopment [1-3]; partly because the assumption that MRI was inherently a safe procedure had reduced theimportance of the publication of negative results [4].Since the introduction of MRI as a clinical modality in theearly 1980s, more than 100,000,000 diagnostic proce-dures (estimated) have been completed worldwide, withrelatively few major incidents [5,6].

Most reported cases of MRI related injuries have beencaused by misinformation related to the MR safety aspects

of metallic objects, implants, and biomedical devices[7,8]. In fact, the MR environment may be unsafe for patients with certain implants, primarily due to move-ment or dislodgment of objects made from ferromagnetic materials [9], but also because of heating and induction of electrical currents, which may present risks to patients

with implants or external devices [10]. These safety prob-lems are typically associated with implants that have elon-gated configurations or that are electronically activated(e.g. neurostimulation systems, cardiac pacemakers, etc.).In the MR environment, magnetic field-related transla-tional attraction and torque may cause hazards to patientsand individuals with such implants. The risks are propor-tional to the strength of the static magnetic field, thestrength of the spatial gradient, the mass of the object, itsshape and its magnetic susceptibility. Furthermore, theintended in vivo use of the implant or device must be

Published: 22 April 2004

BioMedical Engineering OnLine 2004, 3:11

Received: 22 January 2004Accepted: 22 April 2004

This article is available from: http://www.biomedical-engineering-online.com/content/3/1/11

© 2004 Formica and Silvestri; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permittedin all media for any purpose, provided this notice is preserved along with the article's original URL.

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taken into consideration because existing counteracting forces may be present that effectively prevent movement or dislodgment of the object. To date, more than onethousand implants and objects have been tested for MR safety or compatibility. This information is readily availa-

ble to MR healthcare professionals, though it requiresheightened awareness by the MR community to continu-ally review and update their policies and procedures per-taining to MR safety based on the information in therelevant medical literature [11]. Physicians are aware of the absolute contraindications to MRI with regard toimplantable devices, less familiar is the potential for anMRI-induced thermal or electrical burn associated withinduced currents in conductors in contact with thepatient's body. Although detailed studies concerning theburn hazard in MRI have not yet been reported, recent reports have, however, indicated that direct electromag-netic induction in looped cables in contact with the

patient may be responsible for excessive heating [12-14].

A comprehensive presentation and discussion of MR related hazardous effects is beyond the scope of thisreview, thus we will limit the discussion to bio-effects pro-duced by MRI systems acting directly on the human body.

Several research studies have been conducted over the past thirty years in order to assess the potential dangerous bio-effects associated with exposure to MRI diagnostics.Because of the complexity and importance of this issue,most of these works are dedicated to separately examining biological effects produced by a particular magnetic or

electromagnetic field source utilized in MRI. Moreover,the scientific literature proliferates in an ever-increasing number of studies concerning biological effects producedby the interactions of biological matter with electromag-netic fields. Thus, there is a need to integrate and summa-rize the current findings about this topic and, at the sametime, provide the basic knowledge to understand thephysics of the interactions between electromagnetic fieldsand biological systems.

In the present work, after an introduction on the basic principles of MRI systems and the electric and magnetic properties of biological tissues, the basic principles

needed to understand the bio-effects caused by the threemain sources of electromagnetic fields utilized in MRIprocedures are described.

Basic principles of MRI procedures Three different types of electromagnetic fields are utilizedin creating an image based on magnetic resonance:

1. the static magnetic field, , which aligns the proton

spins and generates a net magnetization vector in thehuman body;

2. the gradient magnetic field, which produces different resonant frequencies for aligned protons, depending ontheir spatial positions on the gradient axes; these gradient fields allow for the spatial localization of bi-dimensionalMRI slices and hence the reconstruction of three dimen-sional MRI images;

3. the radio-frequency electromagnetic wave, centered at the proton resonant frequency, which rotates the vector

out of the direction of the static magnetic field; thetime during which the magnetization vector returns to theequilibrium is different for each tissue, and this results in

the two main imaging parameters, T 1 and T 2, whichdirectly relate to the image contrast.

These three fields are essential features of MRI procedures,and each interacts with the electromagnetic properties of biological tissues.

Electric and magnetic properties of biologicaltissuesIt is well known that the electrical properties of biologicaltissues are substantially determined by the electrical inter-actions of polar molecules and ions. Materials composedof neutral molecular dipoles are known as dielectrics,

however, cationic and anionic species in extracellular andintracellular spaces of a living system produce conductivepaths for current flow. Thus, a biological tissue must beconsidered as a conductive dielectric. For this reason, theelectrical behavior of the biological matter can bedescribed by defining two main parameters:

1. the dielectric permittivity, ε, related to the dielectric behavior of the material; and

2. the conductivity, σ, which interacts with the electric

field applied to the tissue ( ).

The current ( ), obtained by Ohm's law, is:

The impedance of living tissue varies, depending on itsdielectric permittivity and conductivity. Therefore, the

value of the current and the attenuation of the electromag-netic field inside the tissue strongly depend on these twoparameters. For biological tissues, both the dielectric per-mittivity and the conductivity are strongly non-linear

B0

M

M

E

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functions of frequency. Moreover, if the frequency of anexternally applied electromagnetic field changes, theinteraction between the field and the tissue also changes.In particular, at low frequencies, electromagnetic fieldsinteract at the cellular or multicellular level; as frequency

progressively increases, bio-electromagnetic interactionsoccur with the cellular membrane and intracellular organelle, followed by molecular interaction and, finally,at microwave frequencies the field interacts only with

water molecules [15].

For these reasons, dielectric permittivity and conductivity show three principal behaviors, also called dispersions,depending on frequency. Figure 1 shows how permittivity and conductivity are strongly dependant on frequency [16] (the frequency range where electromagnetic wavesare used in MR imaging is delineated).Materials that cannot be permanently magnetized are

characterized by a physical parameter, the magnetic sus-ceptibility (χ), which describes their behavior whenplaced in a magnetic field. The response of these materials

when placed in an external magnetic field is to develop amagnetic polarization ( ), measured by the magnetic dipole moment per unit volume, according to theequation:

where ∆τ is the volume containing the microscopic dipole

moments µi. The strength of the magnetic polarization

is locally proportional to the externally applied magnetic

field by the magnetic susceptibility χ, according to the

equation:

and both magnetic fields show a relationship with the

magnetic flux density, , described by the formula:

where µo is the magnetic permeability of vacuum. For

most materials, the induced magnetic polarization is par-

allel to , in this case the materials are called "isotropic."

Thus, χ is a scalar quantity, and vectors , and havethe same direction.

Materials may be classified into three large groups accord-ing to the values of their susceptibility: diamagnetic mate-rials (-1 < χ < 0), paramagnetic materials (0 < χ < 0.01)and ferromagnetic materials (χ > 0.01). Figure 2 shows thespectrum of magnetic susceptibilities, demonstrating that the majority of human tissues is diamagnetic or weakly paramagnetic [17].

Frequency dependence of relative permittivity ε (x) and con-ductivity σ (o); the major dispersion regions α, β and γ areindicatedFigure 1

Frequency dependence of relative permittivity ε (x) and con-ductivity σ (o); the major dispersion regions α, β and γ areindicated. The frequency range of interest for MRI devices isreported. (adapted from Ref. [16])

m

Spectrum of magnetic susceptibilitiesFigure 2Spectrum of magnetic susceptibilities. The figure shows thatthe majority of human tissues is diamagnetic or weakly para-magnetic. (from Ref. [17])

m

ii=∆∆ →

∑limτ

µ

τ0

m

H

m H= ⋅χ

B

B H m= ⋅ +( )µ0

H m

B

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Biological effects of the static magnetic field The safety issues associated with exposure to static mag-netic fields have been discussed for more than a century:in 1892 Peterson and Kennelly [18] studied the effects of the exposure to the largest magnet then available (approx-

imately 0.15 T). They exposed a dog and a young boy tothe whole-body magnetic field, finding no positiveresults. About 30 years later, in 1921, Drinker and

Thompson [19] investigated possible health conse-quences of exposure to magnetic fields in industrial work-ers. They performed numerous experiments in vitro, onnerve-muscle cells, and in vivo, on living animals, andthey concluded that the static magnetic field had no sig-nificance as a health hazard. Since then, several studieshave been performed, and a review [20], published in1962, collected about 400 reports dealing with biologicaleffects of magnetic fields. According to Schenck [17], theportion of this literature dealing with supposed patholog-

ical or therapeutic effects of magnetic fields is contradic-tory and confusing. Moreover, basic information, such asthe field strength and its variation over the body, is not provided.

Interest in the biological effects of static magnetic fieldshas increased with the invention of MRI at the beginning of the 80s. In the last twenty years, several studies werecarried out in order to understand the potential hazardsassociated with exposure to a strong static magnetic field.

The majority of these studies did not report positiveresults, thus postulating no adverse effects for humanhealth. In 1981, Budinger [21] summarized the work

done previous to that date, concluding that from an anal- ysis of the vast literature on cell cultures, animals, andmen, no experimental protocol was found that, whenrepeated by other investigators, gave reproducible positiveresults. Twenty years later, Schenck [17] confirmed thisand concluded his review stating that, because of the dif-ficulty in establishing a negative conclusion, it should not be concluded that it has been proven that there are no sig-nificant biological effects of static magnetic fields. How-ever, the steadily increasing capability to realize ever stronger magnets gives reason to believe that such effectscould eventually be established, but probably at fieldstrengths well above those currently utilized in MRI. In a

relatively recent report [22], no adverse biological effects were found after sub-chronic (10 weeks) exposure to a very high magnetic field (9.4 T) in adult male and femalerats and in their progeny.

In the current literature, only some sensory effects havebeen found associated with exposure to a static magnetic field. There was a statistically significant (p < 0.05) finding for sensations of nausea, vertigo, and metallic taste in sub-jects exposed to 1.5 and 4 T static magnetic fields, but nostatistical significance was found for other effects such as

headache, hiccups, tinnitus, vomiting, and numbness. A higher incidence of positive reports originated from thosesubjects exposed to the 4 T field. However there was noevidence that these effects were at all harmful [23].

Few studies have reported dangerous effects for humanhealth, but such studies have neither been confirmed nor confuted by successive work. For instance, it was reportedthat the auditory evoked potentials of a subject exposed toa static 0.35 T magnetic field was phase-shifted [24]; thephase shift slowly (15 minutes) returned to normal after termination of the magnetic exposure. However, further studies did not confirm these findings [25,26].

Research carried out by Pacini, et al. in 1999 [27]described the effects of the static magnetic field generatedby a 0.2 T magnetic resonance tomograph on a normalhuman neuronal cell culture. They observed that after 15

minutes exposure, cells showed dramatic changes of mor-phology, developing branched dendrites featuring synap-tic buttons. Some modifications in the physiologicalfunctions of cells were also reported, but, here too, thesefindings have not yet been confirmed.

We might conclude that, by examination of current litera-ture and within the limits of our knowledge, the only health hazards to patients significantly associated with theexposure to static magnetic fields are related to the pres-ence of ferromagnetic materials or cardiac pacemakers[28-30]. Although there is no evidence of health hazardsassociated with exposure of patients to strong static mag-

netic fields, we report here several physical mechanisms of interaction between tissues and static magnetic fields that could lead to potential pathological effects.

Flow and motion-induced currents in tissues

As reported above, the current density flowing in bio-

logical tissues exposed to an external electric field, , is

determined by the Ohm's law: , where σ is the

electrical conductivity. If the tissue moves with a velocity

, and it is exposed to a static magnetic field , there is

an additional term in the expression of the electric current

density flowing in the tissue described by the equation:

The term can be seen as a motion-induced electric

field, and it can produce biological effects by disrupting physiological electrical signals of the human body, suchas neuronal conduction and biopotentials. It was reported[31] that ECGs of monkeys exposed to a strong static mag-netic field showed field-induced morphological changesin T-wave shape. It was suggested that this might indicate

J

E

J E= ⋅σ

v

B

J E v B= ⋅ + ×( )σ

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a biological effect on the electric activity of the heart.However, afterwards, these changes were explained by thepresence of the electromotive force (EMF) induced by blood flow in a static magnetic field, which is propor-

tional to the quantity [32,33]. The effects of EMF on

the stimulation of nerve or muscle cells have recently beenstudied in humans at field strengths as high as 8 T [34]. At the highest field strengths currently available, the flow-induced current densities are below the threshold levelsneeded to cause nerve or muscle stimulation effects, andno significant vital sign changes, e.g., ECG recordings,have been reported at these high field strengths [35].

Magnetic effects on chemical reactions The metabolic functions of human tissues require a largequantity of chemical reactions, and it is therefore reason-able to suppose that a strong magnetic field might alter the rates or the equilibrium conditions of these reactions.

For example, if the products of a chemical reaction aremore paramagnetical than the reactants, the presence of amagnetic field could shift the reaction equilibrium toincrease the concentration of the products. A very com-mon and important chemical reaction in humans is thedissociation of oxyhemoglobin (diamagnetic) into sepa-rate molecules of oxygen and hemoglobin (both para-magnetic). In this case, an externally applied magnetic field could lower the energy barrier for the dissociation.Calculations indicate that, even in an applied field of 1 T,the free energy barrier to dissociation is changed by only 1 J/mol [36]. Such a small energy shift has less effect onthe reaction equilibrium than does a temperature change

of 0.01°C.

Another chemical effect of the static magnetic field con-sists of the modification of the kinetics and recombina-tion of radical pairs reactions. Free radicals are supposedto be involved in harmful reactions in biological systems,thus any effect that might increase their reactivity or con-centration could produce or enhance a harmful effect [37]. From this observation, the radical pair mechanismhas been proposed as a working hypothesis for possibleadverse effects of magnetic fields on biological systems. Infact, according to the most accepted theory [38-40], themagnetic field splits the radical pairs into two energy lev-

els, this increases the amount of radicals pairs that escapethe recombination reaction [41], i.e., the concentration of free radicals. Experimental research has shown that weak magnetic fields may reduce the second-order decay rateconstant of the reaction [42]. Several studies analyzed theeffects of magnetic fields on the recombination reactionof radical pairs in micelles and confirmed that an exter-nally applied magnetic field increases the number of rad-icals escaping the recombination reaction [37,39,43].However, few studies have been performed on biologicaltissues or on animals and humans. Claims that low mag-

netic fields damage health have led to extensive medical,chemical and physical research: though no firm evidenceof hazards has emerged [44].

Magneto hydrodynamic forces and pressure

When a static magnetic field is applied to a biological tis-sue, and ionic currents are present, a net force, whose vec-

tor can be calculated as , is applied to the moving

ions.

Although these forces principally act on flowing liquids,such as blood, research has shown there is no requirement for increased cardiac activity in order to maintain a con-stant cardiac output when an external magnetic field isapplied to the body [45,46]. On the other hand, a very small magneto- hydrodynamic force operating on theendolynphatic tissues of the inner ear may be the sourcefor the sensations of nausea and vertigo sometimes

reported at higher field strengths [23,36].

Biological effects of time-varying gradient fieldsDuring an MRI examination, the gradient magnetic fieldsare often switched on and off; for this reason, the time-

variation of the magnetic field ( ) induces into the

patient an electric field ( ), according to Maxwell's thirdequation:

These gradient-induced electric fields, at sufficiently high values, could stimulate nerves and muscles and, at very high levels could generate cardiac stimulation or even

ventricular fibrillation [47]. To help protect patients fromthese potential health hazards, several researchers havedeveloped theoretical models and collected animal andhuman experimental data in order to formulate appropri-ate safety standards. In 1985, Bergeron [48] proposed anassessment of the threshold of peripheral nerve stimula-tion as a valuable indicator of high gradient-induced elec-tric fields. According to this methodology, patients couldbe protected from gradient-induced ventricular fibrilla-tion by not exceeding these thresholds.

Reilly applied his electrode numerical stimulation modelsto determine gradient-induced nerve [49] and cardiac stimulation thresholds [50,51], and predicted electric field amplitudes required for stimulation as a function of

waveform (pulse duration, waveshape, and pulse trainlength). Reilly simulated the patient as an uniform cylin-der with radius R = 0.2 m and with the axis parallel to the

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∂

∂

B

t E

∇ × = − ∂

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static magnetic field . Thus, the value of the z-gradient

induced electric field was calculated by the formula:

S being the cross sectional area of the cylinder. If the z-gra-dient magnetic field is normal and uniform over the areaS, the integral equation is easy to solve, and the strength

of the electric field depends on the time-variation of the

magnetic field ( ) and on the radius of the cross sec-

tional area R, by the formula:

Reilly compared the values of the electric field obtained by his model with the experimental results reported in the lit-erature and suggested that the best approximation for nerve stimulation threshold was an exponential curve. A

better approximation might have been made using anhyperbolic form, which appears to be a better fit for morerecent experimental data [52,53]. Thus, it was estimatedthat the mean cardiac stimulation threshold was a factor of 2 above that of the most sensitive population percentile(1%), and the mean threshold for cardiac fibrillation wasestimated to be another factor of 2.5 above the mean for cardiac stimulation. Figure 3 shows the mean thresholdsfor peripheral nerve and cardiac stimulation for the most sensitive population percentile. If the ramp duration of the time-variation of the magnetic fields is less than 1000

µs, the margin between nerve and cardiac thresholds islarge, but if ramp duration exceeds a few milliseconds, themean peripheral and the cardiac nerve stimulation thresh-olds approach each other [54].

In addition to theoretical models, several studies in vivohave been performed to obtain gradient-induced stimula-tion thresholds in animals and in humans. Bourland, et al. [55-57] and Nyenhuis, et al. [58] found strength-dura-tion curves for gradient-induced nerve stimulation indogs. These studies included both z and transverse gradi-ent coils, with and without the presence of a 1.5 T static magnetic field. The lowest stimulation thresholdsobserved were for peripheral nerve, and at these thresh-olds muscle twitching also was observed. The stimulationthresholds found, were not significantly different at 0 T compared with 1.5 T exposure and, when corrected for pulse shape and pulse train length, appeared to agree

roughly with the Reilly model [49] for the induced electric field required for stimulation.

Bourland, et al. [55,57] also found the mean threshold for magnetic stimulation of respiration and for gradient-induced cardiac stimulation in dogs. It was observed that stimulation thresholds for respiration were approximately three times the mean peripheral nerve stimulation thresh-olds, and that the cardiac stimulation thresholds wereabout nine times greater than the mean peripheral nervethresholds for a ramp duration of 530 µs. In those studiesthey also reported that the energy stored in the gradient magnetic field required for the mean cardiac stimulation

threshold in the dog at 530 µs is 80 times the energy required for the mean peripheral stimulation threshold.Recalling Reilly's estimate that the cardiac stimulationthreshold for the most sensitive population percentile[51] is half the mean, and recognizing that the storedenergy in the gradient magnetic field is proportional tothe square of the magnetic field strength, thus, cardiac stimulation in the most sensitive population percentileshould require 20 times the energy needed for the periph-eral nerve stimulation mean. Finally, in these studies nosignificant differences were observed with or without astatic magnetic field of 1.5 T, and whether cardiac stimu-lation experiments were done with blocked or beating

hearts.

In addition to the studies on animals, several investigatorscarried out gradient-induced stimulation experiments inhumans: among them, Budinger [59], Cohen [60],Schaefer [61,62], Bourland [63] and Ham [64]. A review in 2000 by Schaefer, et al. [47] collected the experimentaldata obtained in these studies and compared the different results reported. In figure 4 we show the experimentaldata points obtained for the z gradient, along with Reilly'sestimate as a curve fit. Reilly's model fits experimental

The mean peripheral nerve stimulation thresholds and car-diac stimulation thresholds for the most sensitive populationpercentile estimated by ReillyFigure 3The mean peripheral nerve stimulation thresholds and car-diac stimulation thresholds for the most sensitive populationpercentile estimated by Reilly. (adapted from Ref. [47])

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data in the 100–1000 µs range, which is currently typicalof clinical MRI work.

Also, the probability of cardiac stimulation assuming dB/dt levels at the mean peripheral nerve stimulation thresh-old was estimated [47]. As shown in figure 5, for gradient ramp durations shorter than 1000 µs, the probability of cardiac stimulation in patients, at the peripheral nervestimulation threshold, is very low (from 10 -29 for 100 µsto 10-10 for 1000 µs). Thus, the stimulation probability increases with gradient ramp duration and, as the number of patients receiving MR scans annually approaches 107, it is important to maintain stimulation probabilities well

below 1/107.

From these findings, Schaefer. et al. [47] proposed to pro-tect patients with the safety standards (developed by theInternational Electrotechnical Commission) reported intable 1. Recently, a study found no significant correlationbetween gross anatomical measurements; such as age,

weight, height, average body and fat percentage; andperipheral nerve stimulation [65].

Biological effects of radiofrequencyelectromagnetic wavesDuring an MRI exam, the patient is exposed to an electro-

magnetic radiation in the range of 8.5 to 340 MHz. This isknown as the radiofrequency (RF) range of the electro-magnetic radiation spectrum, and is nonionizing, that isto say the photons associated with this radiation fre-quency (wavelength) have insufficient energy to ionisethe atoms of biological matter and hence possibly causedamage at the cellular level.

For this reason, while ionizing radiation can cause discreteincreases in the energy of a molecular or atomic absorber,causing irreversible alterations in atomic configurations,

such as ionization or covalent bond disruption, nonioniz-ing radiation (such as radiofrequency electromagnetic

waves) cannot induce irreversible alterations in living sys-tems via single-photon quantized molecular interactions,but only via multiphoton absorption, i.e. direct heating [15].

Another distinction can be made between electromagnetic waves in the "far-field region" and electromagnetic waves

in the "near-field region." In the first case, if the distancefrom the source of the electromagnetic radiation (L) isgreater than the wavelength of the electromagnetic wave(λ), i.e. L >> λ, the electromagnetic radiation may be rep-resented as a propagating wave consisting of transverseelectric (E) and magnetic (H) fields, where the ratiobetween E and H is equal to the "wave impedance" in themedium (this is known as the plane-wave approxima-tion). In the second case, if L is less than or equal to λ, it is possible to use the "quasi-static" approximation, andthe electric and magnetic fields are effectively separable,meaning that the field from a particular source in the"near-field region" is either primarily electric (E >> H) or

magnetic [15,66,67].

In an MRI examination, the patient is in the "near-fieldregion," so biological effects of the radiofrequency electro-magnetic waves are primarily caused by the magnetic field, with negligible contribution of the electric field [68].

Biological effects caused by radiofrequency electromag-netic waves can be grouped into two main categories:

Mean human nerve stimulation thresholds by z gradient; infigure are shown the experimental data and the Reilly fitFigure 4Mean human nerve stimulation thresholds by z gradient; infigure are shown the experimental data and the Reilly fit.(adapted from Ref. [47])

Estimated probability of cardiac stimulation assuming dB/dtlevels are at the mean peripheral nerve stimulationthresholdsFigure 5Estimated probability of cardiac stimulation assuming dB/dtlevels are at the mean peripheral nerve stimulation thresh-olds. (adapted from Ref. [47])

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• Thermal effects, due to tissue heating caused by direct absorption of energy from the electric fields, and by

induced currents as a consequence of Faraday's law [66]. These effects constitute the basis of contemporary interna-tional safety guidelines, also known as the ICNIRP Guide-lines [67];

• Non-thermal effects, which are due to an as yet unknown mechanism of direct magnetic field-tissue inter-action [66].

As for thermal effects, the temperature increase of biolog-ical tissue rises from direct radiofrequency energy absorp-tion. The deposition and distribution of energy within thebody is highly non-uniform and depends on the fre-

quency range of the incident electromagnetic radiation. Asfor energy absorption properties of the human body, elec-tromagnetic frequency spectrum can be divided into four ranges [67]:

1. from 100 kHz up to 20 MHz, the absorption in thetrunk decreases rapidly with decreasing frequency and sig-nificant absorption may occur in the neck and legs;

2. form 20 MHz up to 300 MHz, relatively high absorp-tion can occur in the whole body, and to even higher val-ues if partial body resonances are considered;

3. from 300 MHz up to several GHz, significant local, nonuniform absorption occurs;

4. above 10 GHz, energy absorption occurs primarily at the body surface.

It must be noted that electromagnetic waves normally uti-lized in MRI techniques are in the second range of absorp-tion, at which high absorption occurs in the whole body.

The dosimetric term utilized to describe the absorption of radiofrequency energy is the specific absorption rate

(SAR), which it is normally measured in W/kg. However,especially for human subjects, measurements or estimatesof the SAR levels are not trivial, because body SAR during an MRI examination is a complex function of several var-iables, including the frequency, the type of RF pulse usedand its repetition time, the configuration of the anatomi-cal region exposed, and other factors [69-71].

Numerous studies carried out over the past 35 years haveindicated that the exposure to radiofrequency radiationmay produce various physiological effects, due to RFenergy-induced heating in tissues, including those associ-ated with alterations in visual, auditory, endocrine, neu-

ral, cardiovascular, immune, reproductive, anddevelopmental functions [68].

Several of these studies have been carried out on labora-tory animals to determine thermoregulatory reactions of living systems to tissue heating associated with exposureto RF radiation. Nevertheless, these experiments do not apply directly to the conditions that occur during MRIprocedures, because the pattern of RF absorption, or thecoupling of radiation to biological tissues, depends on thebody size, on the anatomical features, the duration of theexposure, the sensitivity of tissues, and several other fac-tors. Therefore, the data obtained in experiments with ani-

mals cannot strictly predict thermoregulatory or other physiological changes in human subjects exposed to RFradiation during MR examinations [69,72,73].

In addition to experiments on animals, several modelshave been proposed to predict human responses to the RFenergy that is absorbed by the body in MR procedures [74-76]. Though the major limitation of the proposed modelsis the difficulty to take into account the numerous critical

variables that can affect the thermoregulatory responses of the human subjects (age, amount of subcutaneous fat,

Table 1: Safety standards for time-varying magnetic fields developed by the International Electrotechnical Commission (IEC)

Ramp duration (t) Magnetic field variation (dB/dt)

t > 120 µs

12 µs ≤ t < 120 µs

t < 12 µs

∂

∂

<

B

t

T

S

20

∂

∂ <

( )

B

t

2400

t s

T

sµ

∂

∂ ≤

B

t

T

S200

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physical condition of the subject), more importantly,none of the models have ever been validated by experi-ments performed on humans [67].

For the assessment of the actual thermal response during

an MR procedure, it has been necessary to perform severalexperiments during which volunteers have been continu-ously monitored before, during, and after the MR exami-nation. The main result of these experiments has been theindividuation of some physiological parameters that haveshown a significant response to a thermal load, such assublingual or tympanic membrane temperature (goodindicators of "deep body" or "core" temperature), skintemperature, heart rate, oxygen saturation, blood pres-sure, respiratory rate, and cutaneous blood flow; all theseare important physiological variables that can change inresponse to a thermal load [68].

The first experiment on human thermal response to RFradiation-induced heating during MR procedures was per-formed in 1985 by Schaefer [77]. In this study, tempera-ture changes and other physiological parameters weremonitored in subjects exposed to relatively high whole-body average SARs (approximately 4.0 W/kg). The resultsshowed that there were not excessive temperature eleva-tions or other deleterious physiological consequencesrelated to the exposure.

Further studies were conducted on volunteers exposed to whole-body average SARs ranging from approximately 0.05 W/kg to 4.0 W/kg [78-84]. These experiments docu-

ment that body temperature changes were always lessthan 0.6°C, though there were statistically significant increases in skin temperature, but without serious physio-logical consequences. Furthermore, there were no associ-ated deleterious alterations in hemodynamic parameters,i.e. heart rate, blood pressure, and cutaneous blood flow.

A recent study was carried out in order to determine if theheat induced in a head phantom of biological tissue by typical RF energy associated with an 8T MR system causedexcessive temperature changes. The only noticeable effect found was an inhomogeneus RF distribution in ultra highfield systems (> 4 T) [85].

A study was carried out by exposing volunteers to an MRIprocedure with a whole-body average SAR of 6.0 W/kg [86]. This was the highest level of SAR that human sub-jects have ever been exposed to in an MRI procedure. Thisinvestigation was conducted in both cool (22°C) and

warm (33°C) environments. The temperature of the tym-panic membrane and skin, along with heart rate, bloodpressure, oxygen saturation, and skin blood flow weremonitored before, during, and after exposure to the RFelectromagnetic energy. In the cool environment, there

were statistically significant increases in the tympanic

membrane, abdomen, upper arm, hand, and thigh tem-peratures, as well as skin blood flow. In the warm environ-ment, there were statistically significant increases intympanic membrane, hand and chest temperatures, as

well as systolic blood pressure and heart rate. However, all

the changes of the physiological parameters were withinacceptable safe levels. This finding shows that an MR pro-cedure with whole-body averaged SAR of 6.0 W/kg can bephysiologically tolerated by a subject whose thermoregu-latory function is not compromised [68,86].

Finally, it is necessary to consider those organs that havereduced capabilities of heat dissipation and thus may beinjured by elevated temperatures, such as gonads andeyes. Studies have demonstrated that RF radiation-induced heating may have detrimental effects on testicular functions if the scrotal or testicular tissue temperatureexceeds 38°C [76]. A study [88] measured the scrotal skin

temperatures in volunteers exposed to an MRI procedureat whole-body averaged SAR of 1.1 W/kg. The largest increase in scrotal skin temperature was 2.1°C, and thehighest scrotal skin temperature recorded was 34.2°C, i.e.below the threshold known to impair testicular function[87]. With regard to heating of the eyes during an MR examination, corneal temperatures have been measuredin patients exposed to a MRI of the brain with peak SARsup to 3.1 W/kg [89]. The highest corneal temperature rise

was 1.8°C, and the highest temperature measured was34.4°C. Another study was carried out to examine cornealtemperatures in patients with suspected ocular pathology,exposing the subjects to peak SARs ranging from 3.3 to 8.4

W/kg [90]. The highest corneal temperature measured inthis investigation was 35.1°C. As temperatures measuredin these studies were below recognized safety thresholds,it does not appear that clinical MR procedures have thepotential to cause thermal damage to ocular tissue [68].Finally, we should notice the lack in the current literatureof studies concerning patients with conditions that impair heat dissipation.

RF radiation may also cause non-thermal, field-specific changes in biological systems, that are produced without an elevation in temperature. however, non-thermal effectsof RF electromagnetic waves are not well understood and,

above all, have not been studied in association with theuse of MR system [68]. Those interested in a thorough dis-cussion of this topic are referred to the extensive review by Beers [91]. Here we will limit ourselves to report somequalitative considerations arising from the ever increasing importance of the subject [92]. Undoubtedly, in humanbeings electromagnetic fields play a crucial role in control-ling and maintaining orderly physiological functions.

Thus, a living system is an electromagnetic instrument of great sensitivity; because in the relatively short time for

which humanity has been exposed to man-made electro-

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magnetic waves, there is no evidence of evolutionary immunity against any adverse effects this radiation might have. Whereas the thermal effects arise from a transfer of energy between the external fields and the human tissues,the non thermal effects could arise from a "transfer of

information" from the field to the living system. (A goodexample of the transfer of information from the electro-magnetic field to a living system is the ability of a flashing light, at a certain rate, to trigger seizures in people suffer-ing from photosensitive epilepsy; this effect is due, not tothe brightness of the light, but rather to the frequency of the flash.) This type of interaction might be strongly non-linear and dependent on the frequency of the externalelectromagnetic field. Nevertheless, the ICNIRP Safety Guidelines [67] permit humans to be exposed to electric fields that are over ten times stronger than radiation limitsapplicable to all electronic consumer products presently on the market.

ConclusionsPerhaps the safest component of the MRI exam is thestatic magnetic field. By examination of the current litera-ture, and within the limits of our knowledge, the only health hazards significantly associated with the exposureto static magnetic fields are related to the presence of fer-romagnetic materials or cardiac pacemakers in patients.

Almost all of the more than 100 million MRI exams per-formed since early 1980 were completed without any evi-dence of harmful effects to the patient from the static magnetic field. However, due to the signal to noise advan-tages of high field MRI systems, increases in the static

magnetic field are inevitable.

The second potential source of risk in MRI exams arisesfrom the use of pulsed field gradients. High slew rates cancause peripheral nerve and/or cardiac stimulation to thepatient. However, peripheral nerve stimulation, whichcan be painful although not harmful to the subject, has athreshold lower than the level required for potentially dangerous cardiac stimulation. Present day MR systemstypically operate below nerve stimulation levels thus, at the current state of the art, cardiac stimulation is very unlikely.

RF power deposition represents the greatest risk for patient safety in MRI exams. There is widespread agree-ment among scientists in considering that a local increasein temperature of 1°C in a healthy individual is absolutely free of risk. In MRI exams, an SAR of 8 W/kg could beused, but for short enough exposures so as not to producea more than 1°C core body temperature rise. However, interms of safety, it would be desirable that a clinical MR system be equipped with a sensing phantom that couldshut off the power to the RF source when SAR levels

approach the limits established by international safety guidelines.

From these considerations, our hope is that the knowl-edge of magnetic resonance imaging systems safety can

not only help guide the future design of these instru-ments, but also affect the selection of procedures in order to ensure safe, efficacious, and efficient system operation.

Authors' contributionsDF collected, organized and reviewed the literature. SSconceived of the study and reviewed the literature.

All authors read and approved the final manuscript.

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